investigating the effect of el niño on n itrous oxide ...1 investigating the effect of el niño on...

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Investigating the effect of El Niño on nitrous oxide distribution in the

Eastern Tropical South Pacific

Qixing Ji1, Mark A. Altabet2, Hermann W. Bange1, Michelle I. Graco3, Xiao Ma1, Damian L. Arévalo-

Martínez1, and Damian S. Grundle1,4

1GEOMAR Helmholtz Centre of Ocean Research Kiel, Kiel, 24103, Germany 5 2School for Marine Science & Technology, University of Massachusetts Dartmouth, New Bedford, Massachusetts, USA 3Dirección General de Investigaciones Oceanográficas y cambio Climático, Instituto del Mar del Perú (IMARPE), P.O. Box

22, Callao, Perú 4Bermuda Institute of Ocean Sciences, St. George’s, GE01, Bermuda

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Correspondence to: Qixing Ji ([email protected])

Abstract. The open ocean is a major source of atmospheric warming and ozone depleting gas nitrous oxide (N2O). Intense

sea-to-air fluxes of N2O occur in major oceanic upwelling regions such as the Eastern Tropical South Pacific Ocean (ETSP).

The ETSP is influenced by the El Niño-Southern Oscillation that leads to inter-annual variations of physical, chemical and 15

biological properties. A strong El Niño was developing in this region in October 2015, during which we investigated the

N2O production pathways and, by comparing to previous non-El Niño years, the effects of El Niño on water column N2O

distributions and fluxes. Analysis of N2O natural abundance isotopomers suggested that both nitrification and partial

denitrification (nitrate and nitrite reduction to N2O) were important N2O production pathways. Higher than normal sea-

surface temperatures were associated with a deepening of the oxycline, while the level of sea surface N2O supersaturation on 20

the continental shelf was nearly an order of magnitude lower than those of non-El Niño years. Therefore, a significant

reduction of N2O efflux in the ETSP occurred during the 2015 El Niño event. At both offshore and coastal stations, the N2O

concentration profiles during El Niño showed moderate N2O concentration gradients, and peak N2O concentrations were

deeper than during non-El Niño years; this was likely the result of suppressed upwelling retaining N2O in subsurface waters.

The depth-integrated N2O concentrations during El Niño were nearly twice as high as those measured in non-El Niño years, 25

indicating subsurface N2O during El Niño could be a reservoir for intense N2O effluxes when normal upwelling is resumed

after El Niño.

1 Introduction

The El Niño-Southern Oscillation (ENSO) is a naturally occurring decadal climate cycle that affects the oceanic and

atmospheric conditions across the equatorial Pacific (Philander, 1983). A pronounced effect of ENSO in the ocean is the 30

redistribution of heat flux across the tropical and subtropical Pacific. Generally, the ENSO cycle can be divided into three

Biogeosciences Discuss., https://doi.org/10.5194/bg-2018-453Manuscript under review for journal BiogeosciencesDiscussion started: 6 November 2018c© Author(s) 2018. CC BY 4.0 License.

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phases, El Niño, La Niña and neutral. During El Niño / La Niña years, higher / lower sea surface temperature and deepening

/ shoaling of the thermocline occur in the Eastern tropical South Pacific (ETSP) (Barber and Chavez, 1983). During El Niño

years, upwelling is suppressed in the ETSP, leading to a reduction of upward nutrient fluxes to the surface waters and

decreased primary production (Chavez et al., 2003; Ñiquen and Bouchon, 2004).

The ETSP is an oceanic region with intense sea-to-air flux of nitrous oxide (N2O), a strong greenhouse gas and a potent 5

ozone depleting agent (Ravishankara et al., 2009). Diverse microbial processes involved in the production and consumption

of N2O occur in the ETSP, a major oceanic oxygen minimum zones (OMZs) having wide range of O2 concentrations

spanning sub-nanomolar level at intermediate depths (Revsbech et al., 2009) to atmospheric saturation at the surface. In the

presence of oxygen, N2O is a by-product during the first step of nitrification, i.e. ammonium (NH4+) oxidation to nitrite

(NO2-) (Anderson, 1964). Under suboxic and anoxic conditions, N2O is produced via partial denitrification, i.e. NO2

- 10

reduction and nitrate (NO3-) reduction (Codispoti and Christensen, 1985). The dominant biological sink of N2O in the ocean

is the last step of denitrification where N2O is reduced to N2 under anoxic conditions (Babbin et al., 2015). Recent

investigations suggest that N2O uptake by diazotrophs is a possible N2O sink at the surface waters (Farías et al., 2013;

Cornejo et al., 2015). Its environmental significance awaits further exploration.

Recent modelling efforts have highlighted that the ENSO events could prominently change biogeochemical processes 15

related to nitrogen cycling (Carrasco et al., 2017; Mogollón and Calil, 2017; Yang et al., 2017). During El Niño events in the

1980’s, oceanic N2O fluxes decreased (Cline et al., 1987; Butler et al., 1989), which could be related to changes O2 and

organic matter availabilities that are critical environmental factors regulating N2O production (Elkins et al., 1978; Farías et

al., 2009; Arévalo-Martínez et al., 2015; Kock et al., 2016). Here we report water column nitrogen biogeochemistry, N2O

distribution and natural abundance isotopes during October 2015 when a strong El Niño event (recurrence interval > 10 20

years) was developing (Stramma et al., 2016; Santoso et al., 2017). Stable isotope analyses (15N vs. 14N and 18O vs. 16O) were

used to determine the pathways of N2O production and consumption as outlined previously (Yamagishi et al., 2007; Grundle

et al., 2017). Recent publications of time-series studies focusing on biogeochemical variations in the ETSP (Gutiérrez et al.,

2008; Farías et al., 2015; Graco et al., 2017) and the marine N2O database (Kock and Bange, 2015) allow us to present the

effects of a strong El Niño event on water column hydrography and N2O distributions. 25

2 Materials and Methods

2.1 Field sampling and laboratory measurements

The progress and the strength of El Niño was quantified by the Ocean Niño Index (ONI, Figure 1), defined as the

running 3-month average sea surface temperature anomaly for the Niño 3.4 region in the east-central tropical Pacific (5˚S –

5˚N, 120˚W – 170˚W). The 2015-16 El Niño was an “extreme El Niño event” indicated by ONI ≥ 0.5 °C. The ASTRA-OMZ 30

SO243 cruise on board the R/V Sonne took place between the 5th and 22nd October 2015 from Guayaquil, Ecuador to


3

Antofagasta, Chile (Figure 2a). In October 2015, the El Niño was still developing with ONI = 2.1°C, comparable to other

strong El Niño events in 1972-73, 1982-83, 1997-98 (Stramma et al., 2016).

The sampling stations are categorized into offshore (Figure 2a in red polygon) and coastal (Figure 2a white polygon)

according to their respective water depth: The coastal stations are shallower than 250 m whereas the offshore stations are >

3000 m in depth. Water samples were taken from a 24 x 10L bottle CTD-rosette system. At every station, CTD-Niskin 5

bottles collected water samples at approximately 10 – 20 depths spanning the observed oxygen concentration range. The

CTD system was equipped with two independent sets of sensors for temperature, conductivity (salinity) and oxygen

measurements. Calibration for temperature, salinity and oxygen measurements were reported previously, with standard

deviations of 0.002°C, 0.0011 PSU, and 0.8 μmol L-1 [O2], respectively (Stramma et al., 2016). The detection limit of

dissolved oxygen was ~ 3 μmol L-1; the ODZ was operationally defined as water parcels with [O2] < 5 μmol L-1, and the 10

boundary of oxygenated layer was defined as [O2] = 20 μmol L-1. Dissolved NO3- and NO2

- concentrations were measured at

sea with an auto-analyzer (QuAAtro, Seal Analytical, Germany). The detection limit for NO3- and NO2

- was 0.1 and 0.02

μmol L-1, respectively. For N2O concentration measurements, triplicate samples were collected in 20 mL glass vials and were

crimp-sealed with butyl stoppers and aluminum caps. Immediately following this, a 10 mL helium headspace was created

and 50 μL of saturated mercuric chloride (HgCl2) solution was added. After an equilibration period of at least 2 hours the 15

headspace sample (10 mL) was measured by a gas chromatograph equipped with an electron capture detector (GC/ECD).

The GC was calibrated on a daily basis using dilutions of two standard gas mixtures. The detailed GC/ECD setup and

calculation of N2O concentration were reported previously (Walter et al., 2006; Kock et al., 2016).

Samples for natural abundance N2O isotopes were collected and preserved with 100 μL of saturated HgCl2 in 160 mL

glass serum bottles with butyl stoppers and aluminum seals. Isotopic measurements of N2O were carried out at the 20

University of Massachusetts Dartmouth following procedures previously reported (Grundle et al., 2017). In brief, dissolved

N2O was extracted by an automated purge-and-trap system and concentrated with liquid nitrogen. Interfering molecules such

as H2O and CO2 were isolated from N2O to increase measurement precision. A multi-collector isotope ratio mass

spectrometer detected NO+ fragment of N2O (mass 30, 31, for δ15Nα) and intact N2O molecule (mass 44, 45 and 46, for

δ15Nbulk and δ18O). 25

2.2 Data Analysis

Water column N2O saturation was quantified by the N2O excess (ΔN2O), defined as the concentration difference

between measured and equilibrium values:

2 2 2N O N O N Omeasured equilibrium

(1)

The N2O equilibrium concentration was calculated according to Weiss and Price (1980) with in-situ temperature, salinity and 30

the atmospheric N2O dry mole fraction in the year of 2015, 328 ppb at 1 atmospheric pressure (Blasing, 2016).


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The N2O efflux from the ocean to the atmosphere was calculated as the product of N2O excess and gas transfer

coefficient (kw, cm hr-1) that was derived according to empirical relationship proposed by Wanninkhof (2014):

0.52

100.251 660wk U Sc

(2)

where U10 denotes wind speed (m s-1) at 10 m above sea surface, Sc denotes the Schmidt number for N2O under in-situ

temperature (Wanninkhof, 2014). 5

The notations for N2O isotopomer ratios (δX) are defined as the relative difference between isotopic ratio (R) of sample

and reference material:

1sample

reference

RX

R

(3)

where X denotes 15Nα, 15Nβ and 18O, R denotes the 15N/14N at the central (α), terminal (β) and 18O/16O at oxygen positions of

the N2O molecule (see supplementary). Furthermore, the δ15Nbulk (conventionally δ15N) and site preference (SP) are defined 10

as follows:

15 15

15

2bulk

N NN

(4)

15 15

2

N NSP

(5)

The value of δX is expressed as permil (‰) deviation relative to a set of reference materials: atmospheric N2 for δ15Nbulk

δ15Nα and δ15Nβ (Mohn et al., 2014), and Vienna standard mean ocean water (VSMOW) for δ18O. 15

2.3 Additional datasets

The twice-weekly, 50-km resolution of sea surface temperature anomaly from NOAA’s Satellite Coral Bleaching

Monitoring Datasets (https://coralreefwatch.noaa.gov/satellite/ methodology/methodology.php) were used to quantify the

sea-surface temperature difference of the ETSP during October 2015 relative to 1985 – 1993. For N2O flux calculations,

instantaneous wind speed data at each of our sampling locations were acquired from shipboard metrological measurements. 20

Seawater N2O and oxygen concentrations from previous sampling campaigns in the ETSP were extracted from the

MEMENTO database (Kock and Bange, 2015). Specifically, data from the following cruises were used for comparison

between El Niño and non-El Niño years: NITROP-85 (February 1985), M77/3 (January 2009), Callao Time Series Transect

(October 2011), M90 (November 2012), M91 (December 2012), AT26-26 (January 2015). The ONI of these years (1985,

2009, 2011, 2012, Figure 1) indicated that, 1985 and 2011 are considered as weak “La Niña” years, whereas 2009 and 2012 25

are considered “neutral” years.


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3 Results

3.1 Hydrography, distribution of oxygen and inorganic nitrogen

An extreme El Niño event during 2015-16 impacted the ETSP with a relatively high sea surface temperature anomaly,

especially at the equatorial region (2°S – 2°N and 80 – 90°W) where the highest anomaly between 3 and 5°C was observed

at offshore waters (Figure 2a). The El Niño-induced warming effect decreased southwards. Between 5°S and 12°S, the 5

temperature anomaly was 2 – 3°C. South of 12°S the anomaly was generally < 1°C. The shelf areas (7°S – 14°S) had a

progressively lower temperature anomaly southwards; > 1.5 °C and < 1 °C north and south of 12°S, respectively.

Five water masses, based on their thermohaline indices (Strub et al., 1998; Silva et al., 2009) were identified (Figure

2b). The northward-flowing Antarctic Intermediate water (AAIW, T = 3 – 5 °C, S ≈ 34.5) was found at depths below 1000

m. The Equatorial subsurface water (ESSW, T = 8 – 12 °C, S = 34.7 – 34.9) was near the Peruvian coast at depths between 10

300 and 400 m. Above the continental slope (water depth < 250 m), the colder Peru coastal water (PCW, T < 19°C, S ≈ 35)

occupied 30 – 250 m, whereas the warmer subtropical surface water (STSW, T > 18.5 °C, S > 34.9) was found at depth < 30

m. The surface water north of the equator consisted of the tropical surface water (TSW), which had high temperature and

low salinity (T > 25 °C, S < 33.5) due to excess precipitation.

Along the offshore section, the upper oxycline boundary ([O2] = 20 μmol L-1 isoline) was at 250 – 300 m along the 15

equator at 85.5°W, and the ODZ ([O2] < 5 μmol L-1) appeared near 10°S (Figure 3a). The southward shoaling of the

oxycline, thickening of the ODZ and shoaling of the isoline with [NO3-] = 20 μmol L-1 were observed south of 10°S (Figure

3a and 3b), where the thickness of the ODZ was ~ 300 m. The top of the ODZ reached ~125 m between 13°S and 16°S.

Significant accumulation of NO2- (>1 μmol L-1) occurred south of 10°S between 30 and 400 meters within the ODZ (Figure

3c), corresponding to lower NO3- concentrations (Figure 3b). The highest NO2

- concentration (9.4 μmol L-1) was recorded at 20

200 m at 15.7°S.

Along the coastal section, the surface (upper 10 m) O2 concentrations were below saturation at all sampling stations (50

– 97 % saturation, calculated according to Garcia and Gordon (1992)). Surface O2 concentrations were 165 – 217 μmol L-1

north of 10°S and gradually decreased to 135 – 190 μmol L-1 between 10°S and 12.5°S, and to 120 μmol L-1 south of 14 °S

(Figure 3d). The shoaling of the 20 μmol L-1 O2 isoline was observed south of 9°S. The top of the ODZ was found at 200 m, 25

150 m and 80 m at 11°S, 12°S and 14°S, respectively. The surface NO3- concentrations were 11 – 23 μmol L-1 between 9°S

and 16°S, and the 20 μmol L-1 NO3- isoline was at 0 – 20 m (Figure 3e). Water column NO2

- concentrations at coastal

stations were generally below 1 μmol L-1, with the exception of the station at 14.0°S where NO2- concentrations reached 1.2

μmol L-1 below 200 m (Figure 3f).

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3.2 Water column N2O concentrations and isotopes

Along the offshore section, the water column N2O distributions showed a southward increase of surface N2O

concentrations and southward decrease of subsurface N2O maxima (Figure 4a). The equatorial region (1°N to 2.5°S,

85.5°W) had subsurface high N2O concentrations (up to 93 nmol L-1) at intermediate depths (200 – 550 m); water column

δ15N, SP and δ18O generally increased with depth (Figure 4b, 4c and 4d); at the subsurface N2O concentration maximum, 5

δ15N, SP and δ18O were ~ 6 ‰, 13 – 17 ‰, and 45 – 50‰, respectively. Two N2O concentration maxima were observed at

stations south of 10°S where the ODZ was formed. Near 10°S, two N2O concentration maxima (70 ± 6 nmol L-1) occurred

between 200 and 600 m; and a local concentration minimum (~ 30 nmol L-1) occurred within the ODZ at 400 m, associated

with high δ15N (8 – 10 ‰), SP (20 – 30‰) and δ18O (60 – 70‰). Near 13°S, a shallow N2O concentration maximum (~ 80

nmol L-1) occurred at ~100 m, and a local N2O concentration minimum (18 nmol L-1) occurred at 350 m. Between 14°S and 10

16°S, the lowest (< 10 nmol L-1) N2O concentrations were observed at 200 – 400 m within the ODZ, where the highest

values of δ15N (> 10 ‰), SP (30 – 40‰) and δ18O (> 60 ‰) were observed.

Along the coastal section, a southward increase of surface N2O concentration (20 nmol L-1 north of 11°S and > 40 nmol

L-1 south of 13°S) was observed, coinciding with southward shoaling of the ODZ (Figure 4e). Subsurface maximum N2O

concentrations were observed below 200 m near 10.7°S, and at 80 – 90 m south of 12°S, where ODZ was formed. The δ15N 15

in coastal waters were between 2.5 and 5 ‰, with lower values at stations south of 14 °S (Figure 4f). SP was lower (< 0 ‰)

at the surface (< 10 m) near 9°S and at 50 – 150 m near 11 °S; higher SP (10 – 20 ‰) was observed south of 14°S (Figure

4g). The δ18O values were 45 – 60 ‰; higher δ18O (> 55 ‰) were observed within the ODZ below 200 m at 14 °S and below

100 m at 15.3 °S (Figure 4h).

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3.3 Excess N2O and N2O flux to the atmosphere

Both the offshore and coastal stations showed N2O supersaturation in the top 10 m of surface water, and coastal

stations had higher ΔN2O concentrations (15 – 50 nmol L-1) than those of offshore stations (4 – 8 nmol L-1). Subsurface

ΔN2O along the offshore section had higher concentrations (70 – 80 nmol L-1) at the equatorial regions than ΔN2O

concentrations (40 – 60 nmol L-1) at stations located south of 10°S (Figure 5a). Near 15°S, subsurface N2O undersaturation 25

was observed; ΔN2O concentrations were -4 – 0 nmol L-1 at intermediate depths (200 – 400 m) within the ODZ ([O2] < 5

μmol L-1). Along the coastal section, a southward increase of surface and subsurface (50 – 200 m) ΔN2O was observed

(Figure 5b). Subsurface maximum ΔN2O concentrations were > 60 nmol L-1, and occurring at the periphery of ODZ (~ 200

m near 10°S and < 100 m south of 12°S). Undersaturation of N2O (ΔN2O < 0) did not occur in any coastal stations. The N2O

fluxes from the coastal stations were 23 – 108 μmol m-2 d-1, nearly two folds of the offshore fluxes (7 – 50 μmol m-2 d-1, 30

Figure 5c). The highest flux occurred at a coastal station at 14.4°S, 77.3°W, coinciding with the highest surface ΔN2O (50

nmol L-1).


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4 Discussion

The ETSP is one of the world’s major OMZs having active N2O production and intense efflux to the

atmosphere (Arévalo-Martínez et al., 2015; Kock et al., 2016). The gradient spanning from fully oxygenated conditions to

anoxia creates suitable conditions for N2O production and consumption, which causes the co-existence of water column N2O

supersaturation and undersaturation (Codispoti and Christensen, 1985). To identify the N2O cycling pathways, we input N2O 5

isotopomer measurements into a simple mass balance model (section 4.1). Quantitative relationships linking O2, NO3- and

N2O were examined to characterize the effect of oxygenation on N2O production from NH4+ oxidation (section 4.2).

Previously measured N2O concentrations from the ETSP (MEMENTO database, Kock and Bange (2015)) were compared to

data from this study to investigate the difference in water column N2O distribution and effluxes between El Niño and non-El

Niño years (section 4.3), which would better constrain the natural variability of N2O cycling in the ETSP. 10

4.1 N2O cycling pathways inferred from natural abundance isotopic and isotopomeric signatures

The analyses of natural abundance isotopomers quantify the substitutions of nitrogen and oxygen isotopes (15N, 14N,

18O and 16O) occurring on the linear asymmetric N2O molecule (Yoshida and Toyoda, 2000), and can be used to identify

potential production and consumption pathways (Yamagishi et al., 2007; Grundle et al., 2017). The production of N2O in an 15

isolated water body follows mass conservation of the respective isotopes. The mass balance model proposed by Fujii et al.

(2013) quantified the isotopic signature of N2O produced within the water mass (δproduced) by the linear regression of the

inverse N2O concentration (1/[N2O]measured) and the respective isotope values (δobserved):

2

2

1N O

N Oobserved initial produced producedinitial

measured

(6)

where [N2O]initial and δinitial refer to source water N2O concentration and isotopic signature, respectively. It has been shown 20

that SP is indicative of N2O production pathways, because SP is independent of isotopic values of N2O production

substrates; generally, N2O produced via NH4+ oxidation and partial denitrification have distinctive SP values of 30 ± 5 ‰

and 0 ± 5 ‰, respectively (Toyoda et al., 2011). Thus, N2O production processes can be qualitatively characterized by means

of SPproduced. We further identified four water bodies (coastal and offshore stations combined) from shallow to deeper depths

with distinctive features such as O2, NO2- concentrations and depths (Table 1) to discuss N2O cycling pathways as follows. 25

(1) Upper oxycline and surface (Figure S1a): [O2] > 20 μmol L-1. All the samples were from < 200 m (data not shown),

N2O production from this water body could actively contribute to atmospheric efflux. The samples had variable SP values (-

9 – 34 ‰); some coastal samples had the lowest water column SP values ever reported (-9 ‰, Figure 4g). The low SPproduced

(6.4±1.9) indicates that both nitrification and denitrification were sources of N2O to the upper oxycline, with the majority

appearing to come from denitrification. Given that the O2 concentrations were too high for denitrification to proceed locally 30

in the upper oxycline and the surface (Codispoti and Christensen, 1985), the SP signature in this water body was a mixture of


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local nitrification and upwelling/diffusion from suboxic zones of the ODZ proper. Thus, denitrification and nitrification both

contribute to N2O effluxes in the ETSP-OMZ, consistent with a previous study which focused on the coastal regions between

~12 – 14°S (Bourbonnais et al., 2017).

(2) N2O peak (Figure S1b): [O2] < 20 μmol L-1 and [NO2-] < 1 μmol L-1. Generally the samples were from N2O

concentration maxima near the upper boundary of the ODZ. The SPproduced is relatively low (8.3±3.0 ‰) at this suboxic water 5

body ([O2] < 20 μmol L-1), which allowed N2O production from denitrification while inhibited N2O consumption (Bonin et

al., 1989; Farías et al., 2009). With the SPproduced, we conclude that water column N2O maximum was mainly attributed to

partial denitrification (i.e. NO2- and NO3

- reduction), with minor contribution from nitrification. This is consistent with

previous 15N tracer incubation experiments demonstrating the coincidence between local N2O concentration maximum and

high rates of N2O production from NO2- and NO3

- reduction that are 10 – 100 fold higher than the rate of N2O production 10

from NH4+ oxidation (Ji et al., 2015).

(3) Oxygen deficient zone (Figure S1c): [O2] < 5 μmol L-1 and [NO2-] > 1 μmol L-1. Accumulation of NO2

- within the

anoxic layer is prominent feature of ODZ, where N2O consumption occurs (Codispoti and Christensen, 1985). The isotopic

signature of “produced N2O” had distinctively high δ15Nbulk (8.5 ‰), and δ18O (71 ‰, Table 1 and Figure S2), and this is

indicative of N2O reduction to N2 which results in an isotope enrichment of the remaining N2O pool in the process of N-O 15

bond breakage (Toyoda et al., 2017). The SP signature was also high (39.9 ‰). While NH4+ oxidation can produce N2O with

similar SP values, we rule this out given the low O2 concentrations which were observed (Peng et al., 2016). instead, similar

to the high δ15Nbulk and δ18O values which were observed, we suggest that the high SP values which were recorded in the

ODZ, where N2O undersaturation occurred, were also a result of N2O consumption, as reduction of N2O can also result in

high SP values (Popp et al., 2002; Well et al., 2005; Mothet et al., 2013). Based on the observed δ15Nbulk, δ18O and SP values 20

of N2O, we conclude that N2O consumption was the predominant N2O cycling pathway in the water body with [O2] < 5 μmol

L-1 and [NO2-] > 1 μmol L-1 in the ETSP.

(4) Intermediate waters (Figure S1d): Samples from depths 500 – 1000 m. Generally, the N2O concentrations peaks

below the oxygen minimum layer at the offshore waters can be found in this water body (Figure 4a). From the linear

regression, the SPproduced is 15.6±4.1 ‰. The samples had [O2] = 5 – 70 μmol L-1, suitable for N2O production from both 25

nitrification and denitrification. Downward mixing and diffusion from ODZ is unlikely because the ETSP is a major

upwelling region and ODZ samples had high SP values (see next paragraph). We conclude that localized N2O production

from nitrification and denitrification are important pathways in this region of the water column, and probably contributed to

N2O concentrations maxima in intermediate waters, as reported by Carrasco et al. (2017).

There are some limitations of the isotopomers-based analysis of potential N2O production pathways. (1) Constant 30

atmospheric exchange at the surface and mixed layer, and mesoscale eddy activities at intermediate waters (Arévalo-

Martínez et al., 2016) could affect the SPproduced from localized N2O production. Nevertheless our conclusion of

denitrification being important pathway remains valid. As a comparison, water bodies were divided by potential density (i.e.

σθ > 27 kg m-3, 26 – 27 kg m-3, 25 – 26 kg m-3, < 25 kg m-3) and showing SPproduced of 5.0 – 11.1 ‰. (2) The rates of N2O


9

production was not derived due to the lack of complimentary dataset (i.e. nitrate and nitrite isotopes) and thus we are not

able to investigate the change of N2O production rates during nitrification and denitrification that are affected by El Niño-

induced lower export production (in comparison to non-El Niño years, Espinoza-Morriberón et al. (2017)).

4.2 The effect of O2 on N2O production from NH4+ oxidation 5

The oxygenated surface mixed layer is constantly in direct contact with the atmosphere. Thus, N2O production via

NH4+ oxidation is important to oceanic N2O fluxes. During NH4

+ oxidation to NO2-, the effectiveness of N2O production in

oxygenated waters can be quantified with the N2O yield, which is defined as the molar nitrogen ratio of N2O produced and

NH4+ oxidized. In oxygenated waters, the near absence of NH4

+ and NO2- suggest the amount of NH4

+ oxidized produces

equal amounts of NO3- within measurement error. Rees et al. (2011) and Grundle et al. (2012) computed the N2O yield by 10

deriving the slope of the linear regression of ΔN2O-NO3- relationship. The ΔN2O data from all sampling stations during

October 2015 showed that ΔN2O increases with increasing NO3- concentrations and decreasing O2 concentrations (Figure 6).

The samples from the upper oxycline ([O2] > 20 μmol L-1 and depth < 500 m) showed moderate increase of ΔN2O (0 – 20

nmol L-1) when [NO3-] < 20 μmol L-1. At [NO3

-] > 20 μmol L-1, substantial increase of ΔN2O (20 – 75 nmol L-1) was

observed. Here, to avoid sampling the ODZ where suboxic condition stimulates N2O production from partial denitrification, 15

only data from the upper oxycline were used to perform linear regression. The slope of the regression at [NO3-] < 20 μmol L-

1 (corresponding to [O2] > 100 μmol L-1) is 0.85 ± 0.11, indicating that 0.085 ± 0.011 nmol of N2O is produced for every

μmol of NO3- produced (or NH4

+ oxidized), equating to a molar nitrogen yield (mol N2O-N produced / mol NO3- produced)

of 0.17 ± 0.02 %. At [NO3-] > 20 μmol L-1 (corresponding to [O2] < 100 μmol L-1) the yield increases to 0.85 ± 0.13 %.

These N2O yield estimates are generally comparable to previously reported values (0.04 – 1.6 %) in the ETSP (Elkins 20

et al., 1978; Ji et al., 2015), and indicating that potential N2O production from NH4+ oxidation decreases with water column

oxygenation due to intrusion of oxygen-rich water masses (Llanillo et al., 2013; Graco et al., 2017). As discussed earlier, the

oxycline samples were probably influenced by mixing of suboxic water with active denitrification producing high N2O

concentrations and low NO3- concentrations; the N2O yield estimates here are thus spatially and temporally integrated. As a

comparison, 15N tracer incubation method directly measured 0.04 % N2O yield during NH4+ oxidation at [O2] > 100 μmol L-25

1 (Ji et al., 2015).

4.3 N2O distribution and fluxes during El Niño

Excess N2O (ΔN2O) in surface waters is one of the principal factors regulating N2O fluxes. To evaluate the effect of

strong El Niño events on oceanic N2O fluxes, we compare surface and water column ΔN2O concentrations in shelf waters (< 30

300 m depth) along 8 – 16 °S during El Niño (October 2015) and “neutral” conditions (December 2012, from Kock et al.

(2016)). Both data sets revealed that higher surface ΔN2O concentrations and thus higher potential N2O efflux occurred at


10

near-shore waters. Generally, the surface ΔN2O concentrations in October 2015 (Figure 7a) were lower than those of

December 2012 (Figure 7d); highest surface ΔN2O concentrations were 50 and 250 nmol L-1 in 2015 and 2012, respectively.

The region of high surface ΔN2O occurred at near ~ 14°S and ~ 10°S in 2015 and in 2012, respectively. It appears that N2O

efflux was significantly reduced during El Niño; in October 2015, coastal water had N2O flux of 23 – 108 μmol m-2 d-1

(Figure 5c), much lower than that of December 2012 having 459 – 1825 μmol m-2 d-1 (Arévalo-Martínez et al., 2015). 5

Suppressed upwelling or increased downwelling during El Niño events, as observed in both observational and model

studies (Llanillo et al., 2013; Graco et al., 2017; Mogollón and Calil, 2017), can directly and indirectly affect N2O fluxes to

the atmosphere: First, reduced upward transport of subsurface N2O-rich water not only decreased surface ΔN2O, but also

increased subsurface ΔN2O, which is illustrated by the comparative observation of higher subsurface ΔN2O concentrations in

coastal waters in October 2015 (Figure 7b, 7c) than those in December 2012 (Figure 7e, 7f). Second, because the oxygen 10

sensitivity of the denitrification sequence increases with each step (Körner and Zumft, 1989), El Niño-induced water column

oxygenation inhibited N2O consumption within the ODZ (bounded by [O2] = 5 μmol L-1 isoline), as demonstrated by the

disappearance of N2O undersaturation (ΔN2O < 0) in coastal water in 2015 (Figure 7b, 7c), contrasting to water column N2O

undersaturation occurring at 100 m at 13 – 14 °S in December 2012 (Figure 7e, 7f). Third, as shown in this study, the

deepening and expansion of the suboxic zone caused by the El Niño event ([O2] = 5 – 20 μmol L-1) stimulated subsurface 15

N2O production via denitrification, as demonstrated by the close spatial coupling between local maximum ΔN2O

concentrations and the oxycline ([O2] = 5 and 20 μmol L-1 isolines, Figure 7b and 7e). Lastly, upwelling of oxygen-rich

water along the Peruvian coast, especially north of 12°S (Stramma et al., 2016), inhibited local N2O production and caused

the southward relocation of surface ΔN2O “hot spots”.

The decrease of surface ΔN2O concentration during El Niño was associated with an increase of subsurface N2O 20

concentrations. Water column ΔN2O concentration profiles at expanded temporal and spatial coverage (see Figure 2a for

station coordinates) were compared within the same season between El Niño and non-El Niño years (Figure 8). We included

data from January 2015, which had the highest ONI during austral summer than any other years. Generally, subsurface

ΔN2O concentration peaks were observed at deeper depths during 2015. Offshore stations had higher subsurface peak ΔN2O

concentrations during El Niño (Figure 8a, 8b), except at station C where the peak concentration during October 2015 was 25

comparable to that of December 2012 (Figure 8c). At coastal stations D and E, higher ΔN2O concentrations were found

below 50 m but peak ΔN2O concentrations were lower during El Niño years (Figure 8d, 8e). In the southernmost coastal

station F, the peak ΔN2O concentration was higher in 2015 than that of 1985; both were found at similar depths at ~ 60 m.

The increase of subsurface N2O concentrations during El Niño resulted in OMZ water column retaining larger amount of

N2O, as shown by higher depth-integrated N2O concentrations during El Niño years than normal years in both coastal and 30

offshore waters (Figure 9).

In all, the apparent decrease in N2O efflux during the El Niño event in the tropical Pacific, as shown in this study and

others (Cline et al., 1987; Butler et al., 1989) is the result of complex physical and biochemical changes. The above

comparative analyses are simple due to limited data availability. Consequently, these following aspects are yet to be


11

resolved: (1) It is unclear how offshore N2O fluxes vary from “neutral” to El Niño years. Current ΔN2O profiles show higher

surface ΔN2O concentrations at station A and B in 2015 (Figure 8a and 8b), whereas the surface ΔN2O was lower in 2015 at

station C (Figure 8c). A zonal (east-west) section near 12°S showed slightly higher offshore surface ΔN2O in 2015 (~ 5 nmol

L-1, Figure 7c) than in 2012 (~ 1 nmol L-1, Figure 7f). The decrease in coastal N2O fluxes during El Niño could be

compensated by increase in offshore fluxes. (2) The southward relocation of high surface ΔN2O from neutral to El Niño 5

years (Figure 7a and 7d) possibly results in higher surface ΔN2O hence higher N2O flux in southern region of ETSP (e.g.

south of 16°S, Figure 8f). (3) It is possible that once the normal upwelling is resumed after the El Niño event, N2O produced

and retained in the subsurface layer in coastal and offshore waters could be a potential reservoir contributing to high N2O

fluxes. (4) The co-occurrence of El Niño and mesoscale eddy formation along the Peruvian coast will have complicated

effects on N2O fluxes, which remains unexplored. 10

5 Conclusions

The eastern tropical South Pacific Ocean is a major upwelling region that is ideal to study the effect of strong El Niño

events on N2O efflux and associated water column biogeochemistry. During a developing strong El Niño event in October

2015, a more pronounced warming effect occurred at lower latitudes in the ETSP. In comparison to conditions in December

2012 (non-El Niño), the depths of the oxygen deficient zone’s upper boundary at lower latitudes were deeper in October 15

2015, coinciding with lower peak N2O concentrations. Shelf N2O effluxes were significantly lower during 2015 El Niño as a

result of lower surface levels of N2O supersaturation. However, a change of upwelling pattern appeared to cause higher

subsurface N2O concentrations and doubled the depth-integrated N2O concentrations during El Niño than in other non-El

Niño years. Natural abundance isotopic and isotopomer analysis indicated that both nitrification and denitrification are

important pathways for N2O production, and denitrification-derived N2O probably contributes to the efflux to the 20

atmosphere. Decreased N2O efflux and subsurface accumulation during strong El Niño events is likely the result of

suppressed upwelling and water column oxygenation. However, the complex spatial and temporal patterns of El Niño-

induced N2O distribution in ETSP remain to be explored.


12

Figures and tables

Figure 1: Ocean Niño Index of year 1985 (weak La Niña), 2009 (neutral), 2011 (weak La Niña), 2012 (neutral) and

2015 (strong El Niño). Data was downloaded from:

http://origin.cpc.ncep.noaa.gov/products/analysis_monitoring/ensostuff/ONI_v5.php. 5

Figure 2: (a) Monthly mean sea surface temperature anomaly (°C) of October 2015 from NOAA’s Satellite Coral

Bleaching Monitoring Datasets. Sampling stations (filled circles) are categorized as “offshore” (in red polygon) and

“coastal” sections (in white polygon). Comparative analyses of water column N2O (see section 4.3) were performed at

stations A – E (open diamonds). (b) Potential temperature – salinity diagram, with corresponding depths (meters, 10

colour bar on right) and potential density (σθ, kg m-3) of all sampling stations. Five water masses are shown: Tropical

surface water (TSW), Subtropical surface water (STSW), Peru coastal water (PCW), Equatorial subsurface water

(ESSW) and Antarctic intermediate water (AAIW).

Figure 1 Ocean Niño Index of year 1985 (weak La Niña),

2009 (neutral), 2011 (weak La Niña), 2012 (neutral) and

2015 (strong El Niño).

-1.5

-1.0

-0.5

0.0

0.5

1.0

1.5

2.0

2.5

1 2 3 4 5 6 7 8 9 10 11 12

Month of the year

1985 2009 2011 2012 2015

Oce

an

Niñ

o I

nd

ex

( C

)

Figure 2 (a) Monthly mean sea surface temperature anomaly

( C) of October 2015 (a). Sampling stations (filled circles) are

categorized as “offshore” (in red polygon) and “coastal” sections

(in white polygon). In section 4.3, comparative analyses of water

column N2O were performed at stations A – E (open diamonds).

(b) Potential temperature – salinity diagram, with corresponding

depths (meters, color bar on right) and potential density (σθ, kg m-

3) of all sampling stations. Five water masses are shown: Tropical

surface water (TSW), Subtropical surface water (STSW), Peru

coastal water (PCW), Equatorial subsurface water (ESSW) and

Antarctic intermediate water (AAIW).

a

AAIW

ESSW

PCW

TSW

STSW

b

Salinity (‰)

Po

ten

tia

l te

mpe

ratu

re ( C

)


13

Figure 3: Water column oxygen (a and d), nitrate (b and e) and nitrite concentrations (c and f) along the offshore (a,

b and c) and coastal sections (d, e and f) during October 2015. 5

Figure 3 Water column oxygen (a and d), nitrate (b and e) and

nitrite concentrations (c and f) along the offshore (a, b and c)

and coastal sections (d, e and f) during October 2015.

Offshore Coastal

Dep

th (

m)

Latitude

a d

b e

c f

[O2] (μmol L-1)

Nitrate (μmol L-1)

[O2] (μmol L-1)

Nitrate (μmol L-1)

Nitrite (μmol L-1) Nitrite (μmol L-1)


14

Figure 4: Water column N2O concentrations (a and e), δ15Nbulk (b and f), site preference (c and g) and δ18O (d and h)

along the offshore (a, b, c and d) and coastal sections (e, f, g and h) during October 2015. White contour line in (a)

and (e) denote the boundary of oxygen deficient zone ([O2] = 5 μmol L-1 isoline) 5

Figure 4 Water column N2O concentrations (a and e), δ15Nbulk (b

and f), site preference (c and g) and δ18O (d and h) along the

offshore (a, b, c and d) and coastal sections (e, f, g and h) during

October 2015. White contour line in (a) and (e) denote the

boundary of oxygen deficient zone ([O2] = 5 μmol L-1)

Dep

th (

m)

Latitude

a e

Offshore Coastal

b f

c g

d h

[N2O] (nmol L-1) [N2O] (nmol L-1)

N2O - δ15Nbulk (‰) N2O - δ15Nbulk (‰)

N2O – Site preference (‰)

N2O - δ18O (‰)

N2O – Site preference (‰)

N2O - δ18O (‰)


15

Figure 5: N2O excess (ΔN2O, nmol L-1) at the offshore section (a) and the coastal section (b) during October 2015; the

white dashed line indicates the boundary of the oxygen deficient zone ([O2] = 5 μmol L-1 isoline). (c) Surface N2O

efflux (μmol m-2 d-1) from offshore and coastal stations (enclosed in white polygon) during October 2015.

5

Figure 5 N2O excess (ΔN2O, nmol L-1) at offshore section (a) and

coastal section (b) in October 2015; the white dashed line indicates

the boundary of oxygen deficient zone ([O2] = 5 μmol L-1). (c)

Surface N2O efflux (μmol m-2 d-1) from offshore and coastal stations

(enclosed in white polygon) in October 2015.

Dep

th (

m)

Latitude

a

Latitude

Offshore c

b Coastal


16

Figure 6: NO3--ΔN2O relationship for samples from the upper oxycline ([O2] > 20 μmol L-1, depth < 500 m, colored

circles), low oxygen ([O2] < 20 μmol L-1) coastal waters (+), low oxygen offshore waters (open circles), and the lower

oxycline (depth > 500 m, filled triangles). Color bar shows the O2 concentrations (μmol L-1). For samples with NO3- 5

concentrations higher and lower than 20 μmol L-1, two linear regressions were performed separately.

y1 = 0.8471x + 0.0365

r2 = 0.52

y2 = 4.2539x - 69.296

r2 = 0.38

ΔN

2O

(nm

ol L

-1)

[NO3-] (μmol L-1)

Figure 6 NO3--ΔN2O relationship for samples from the upper oxycline

([O2] > 20 μmol L-1, depth < 500 m, colored circles), low oxygen ([O2]

< 20 μmol L-1) coastal waters (+), low oxygen offshore waters (open

circles), and the lower oxycline (depth > 500 m, filled triangles). Color

bar shows the O2 concentrations (μmol L-1). For samples with NO3-

concentrations higher and lower than 20 μmol L-1, two linear

regressions were performed separately.

Offshore, depth > 500m

Offshore, [O2] < 20 μM

Coastal, [O2] < 20 μM


17

Figure 7: Surface ΔN2O (a and d), meridional water column ΔN2O distribution (b and e) and zonal water column

ΔN2O distribution (c and f) in October 2015 and in December 2012. Color bars for ΔN2O (nmol L-1) are shown in d, e

and f. For meridional ΔN2O distribution (b and e), data are from the coastal section, shown as white dashed polygon

in panel (a) and (d). For zonal ΔN2O distribution (c and f), data are from a section 12 – 13°S, shown as white 5

rectangle. In (b) and (e) the “20” contour line (black) denotes the [O2] = 20 μmol L-1 isoline, equivalent to the lower

boundary of oxygenated layer; the “5” contour line (white) denotes the [O2] = 5 μmol L-1 isoline, equivalent to the

upper boundary of oxygen deficient zone.

December 2012October 2015

Figure 7 Surface ΔN2O (a and c) and water column ΔN2O distribution (b and d) in October 2015 (a and b)

and in December 2012 (b and d). Color bars for ΔN2O (nmol L-1) are shown in (c and d). For (b) and (d),

data are from “coastal” section (enclosed in white polygon in panel (a) and (b)). The “20” contour line

(black) denotes the [O2] = 20 μmol L-1 isoline, equivalent to the lower boundary of oxygenated layer; the “5”

contour line (white) denotes the [O2] = 5 μmol L-1 isoline, equivalent to the upper boundary of oxygen

deficient zone.

da

eb

Latitude

ΔN2O (nmol L-1)ΔN2O (nmol L-1)

fc ΔN2O (nmol L-1)ΔN2O (nmol L-1)

Longitude


18

Figure 8: Depth profiles of N2O concentration excess (ΔN2O, nmol L-1) measured at 6 different stations representing

offshore (a, b and c) and coastal waters (d, e and f) during February 1985 (filled squares in f), January 2009 (filled

triangles in e), October 2011 (filled diamonds in d), November 2012 (filled circles in a and b), December 2012 (open

squares in c), January 2015 (open circles in e and f) and October 2015 (crosses). Profiles of 2015 are indicated in red 5

and other years in blue.

Figure 8 Depth profiles of water column N2O excess (ΔN2O, nmol L-1)

measured at 6 different stations representing offshore (a, b and c) and

coastal waters (d, e and f) during February 1985 (filled squares in f),

January 2009 (filled triangles in e), October 2011 (filled diamonds in d),

November 2012 (filled circles in a and b), December 2012 (open squares

in c), January 2015 (open circles in e and f) and October 2015 (crosses).

Profiles of 2015 are indicated in red and other years in blue. See Table 2

and Figure 2a for station coordinates.

De

pth

(m

)

ΔN2O concentration (nmol L-1)

0

200

400

600

800

1000

0 20 40 60 80 100

Station A

Oct. 2015Nov. 2012

0

20

40

60

80

100

-50 0 50 100 150

Station D

Oct. 2015Oct. 2011a d

0

200

400

600

800

1000

0 20 40 60 80 100

Station B

Oct. 2015Nov. 2012

0

200

400

600

800

1000

0 20 40 60 80 100

Station C

Oct. 2015Dec. 2012

0

30

60

90

120

150

-50 0 50 100 150

Station E

Jan. 2015Jan. 2009

0

50

100

150

200

250

0 20 40 60 80 100

Station F

Jan. 2015Feb. 1985

b e

c f


19

Figure 9 Comparison of depth-integrated N2O concentrations between El Niño (red bars) and normal years (blue

bars). Station A, B and C are characterized as offshore stations whereas D,E and F are as coastal stations. See Figure

2a for station locations and Table S1 for references.

5

10

Figure 9 Comparison of depth-integrated N2O concentrations between El

Niño (red bars) and normal years (blue bars). Station A, B and C are

characterized as offshore stations whereas D,E and F are as coastal

stations.

0

10

20

30

40

50

60

70

A B C D E F

Dep

th-i

nte

gra

ted

N2O

co

ncen

trati

on

s

(mm

olm

-2)

Station

(integration depth range)

(0 – 1000 m) (0 – 800 m) (0 – 800 m) (0 – 70 m) (0 – 100 m) (0 – 250 m)

Oct.

201

5

Oct.

201

5

Oct.

201

5

Oct. 2

015

Jan. 2

015

Ja

n. 2

01

5

Nov.

2012

Nov.

201

2

Dec.

2012

Oct. 2

011

Jan. 2

009

Feb

. 19

85

Offshore station Coastal station


20

Table 1: Isotopic signature of produced N2O estimated by linear regression of isotopomer ratios and inverse N2O

concentrations (see section 4.1 for model description and supplementary Figure S1 for results) in ODZ, N2O peak,

oxycline and surface layers.

Layer Definition

δ15Nbulk

(‰)

δ18O

(‰)

SP

(‰)

Upper oxycline

and surface

[O2] > 5 μmol L-1

Depth < 500 m

Produced N2O 2.8 45.9 6.4

Standard error 0.3 1.2 1.9

R2 (n = 76) 0.37 0 0.04

N2O peak [O2] = 5 – 20 μmol L-1

Depth < 500 m

Produced N2O 5.4 41.3 8.3


R2 (n = 48) 0.04 0.24 0.08

Oxygen deficient zone [O2] < 5 μmol L-1

[NO2-] > 1 μmol L-1

Produced N2O 8.5 71.0 39.9


R2 (n = 11) 0.38 0.40 0.01

Intermediate waters Depth = 500 - 1000 m

Produced N2O 3.6 50.0 15.6


R2 (n = 21) 0.69 0 0.04

5

Acknowledgements

The German Federal Ministry of Education and Research (BMBF) grant (03G0243A) awarded to C. Marandino, D.

Grundle and T. Steinhoff supported the ASTRA-OMZ cruise onboard the R/V Sonne in October 2015. The Deutsche

Forschungsgemeinschaft (DFG) provided support via the Sonderforschungsbereich 754: Climate-Biogeochemistry 10

Interactions in the Tropical Ocean and funded the R/V Meteor cruises. The BMBF also supported this study as part of the

SOPRAN project I and II (03F0611A, 03F0662A). We thank the captains and crews of the R/V Meteor and R/V Sonne

cruises for their help, C. Marandino (co-chief scientist) and T. Steinhoff for co-organizing the R/V Sonne cruise with D.

Grundle, and M. Lohmann, H. Campen and M. Sun for the oxygen and nutrient measurements and help with N2O sampling.

We thank the Peruvian authorities for allowing us to conduct work in their territorial waters. We thank Tina Baustian 15

contributing hydrography and N2O data off the Peruvian coast. In preparation of the manuscript, C. Marandino and L.

Stramma provided constructive comments. Ji also received support from a DFG grant awarded to D. Grundle and C.

Marandino.


21

Data availability

Raw data presented in this manuscript can be found in the Supplementary material.

Author contributions

DSG developed the experimental design. HWB, MIG, XM, DLA-M, DSG conducted field sampling. MA, XM, DLA-

M conducted laboratory analyses. QJ and DSG perform data synthesis. QJ, MA, HWB, MIG, XM, DLA-M, DSG prepared 5

the manuscript.

Competing Interests

The authors declare that they have no conflict of interest.

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